Imidacloprid effects on bees

Imidacloprid was first registered in the United Kingdom in 1993 and in the United States and France in 1994.[7] In the mid to late 1990s, French beekeepers reported a significant loss of bees, which they attributed to the use of imidacloprid. In 1999, the French Minister of Agriculture suspended the use of imidacloprid on sunflower seeds and appointed a team of expert scientists to examine the impact of imidacloprid on bees. In 2003, this panel, referred to as the Comité Scientifique et Technique (CST, or Scientific and Technical Committee) issued a 108-page report, which concluded that imidacloprid poses a significant risk to bees.[8] In 2004, the French Minister of Agriculture suspended the use of imidacloprid as a seed treatment for maize (corn). Despite these bans, colony collapse disorder still is occurring.[9]

Like most insecticides, imidacloprid is highly toxic to bees, with a contact acute LD50 = 0.078 μg a.i./bee and an acute oral LD50 = 0.0039 μg a.i./bee.[10] Imidacloprid was first widely used in the United States in 1996 as it replaced 3 broad classes of insecticides. In 2006, U.S. commercial migratory beekeepers reported sharp declines in their honey bee colonies. This has happened in the past; however, unlike previous losses, adult bees were abandoning their hives. Scientists named this phenomenon colony collapse disorder (CCD). Reports show that beekeepers in most states have been affected by CCD.[2] Although no single factor has been identified as causing CCD, the United States Department of Agriculture (USDA), in their progress report on CCD, stated that CCD may be "a syndrome caused by many different factors, working in combination or synergistically."[11]

In a British parliamentary inquiry in 2012, the Environmental Audit Committee accused European regulators of ignoring evidence of imidacloprid risk to bees. The committee said that imidacloprid data available in the regulators' own assessment report shows "unequivocally that imidacloprid breaks down very slowly in soil, so that concentrations increase significantly year after year with repeated use, accumulating to concentrations very likely to cause mass mortality in most soil-dwelling animal life." The committee submitted a lengthy list of failings in current regulations including concerns that current regulations were set up for pesticide sprays, not systemic chemicals like imidacloprid that is used to treat seeds. They also expressed concern that only effects on honeybees have been considered despite the fact that 90% of pollination is carried out by different species, such as bumblebees, butterflies, moths and other insects. The environment minister responded saying that he is presently "...satisfied that the [European regulatory system] is working properly."[12]

Dave Goulson from the University of Stirling has found that trivial effects due to imidacloprid in lab and greenhouse experiments can translate into large effects in the field. The research found that bees consuming the pesticide suffered an 85% loss in the number of queens their nests produced, and a doubling of the number of bees who failed to return from food foraging trips.[13][14]

Researchers from the Harvard School of Public Health write that new research provides "convincing evidence" of the link between imidacloprid and the phenomenon known as Colony Collapse Disorder. Lead author of the study, Chensheng (Alex) Lu, stated that experiments showed a dose of 20 parts per billion of imidacloprid (less than the concentrations bees would encounter while foraging in sprayed crops), was enough to lead to Colony Collapse Disorder in 94% of colonies within 23 weeks.[15][16] The hives were nearly empty and the researchers did not find signs of the Nosema fungus or Varroa mites.[17] The researchers proposed two possible sources of bees' exposure to imidacloprid. The first is through the nectar of plants sprayed with the pesticide itself, which is predicted by researchers at the University of Stirling, U.K., to have widespread impacts as imidacloprid is registered for use on over 140 crops in at least 120 countries.[14] The second is through the high-fructose corn-syrup that most bee-keepers in the United States use to feed their bees. Since application of imidacloprid to corn in the United States began in 2005 cases of Colony Collapse Disorder have grown significantly: from losses of 17% to 20% throughout the 1990s to somewhere between 30% and 90% of colonies in the United States since 2006.[2][18]

In May 2012, researchers at the University of San Diego released a study that showed that honey bees treated with a small dose of imidacloprid, comparable to what they would receive in nectar and formerly considered a safe amount, became "picky eaters," refusing nectars of lower sweetness and preferring to feed only on sweeter nectar. It was also found that bees exposed to imidacloprid performed the "waggle dance," the movements that bees use to inform hive mates of the location of foraging plants, at a lesser rate.[19]

Also in 2012, USDA researcher Jeff Pettis published the results of his study, which showed that bees treated with sub-lethal or low levels of imidacloprid had higher rates of infection with the pathogen Nosema than untreated bees.[20] His research confirmed that done by Alaux (2010) and Vidau (2011), who found that interactions between Nosema and neonicotinoids weakened bees and led to increased mortality.[21][22]

Imidacloprid is one of the most toxic insecticides to the western honeybee, Apis mellifera.[23] The toxicity of imidacloprid to Apis mellifera differs from most insecticides in that it is more toxic orally than by contact. The contact acute LD₅₀ is 0.024 µg a.i./bee (micrograms of active ingredient per bee).[24] The acute oral LD₅₀ ranges from 0.005 µg a.i./bee to 0.07 µg a.i./bee, which makes imidacloprid more toxic to the bees than the organophosphate dimethoate (oral LD₅₀ 0.152 µg/bee) or the pyrethroid cypermethrin (oral LD₅₀ 0.160 µg/bee).[23] Other insecticides that are equally or more toxic than imidacloprid include spinosad,[25] emamectin benzoate, fipronil, and the neonicotinoids clothianidin, thiamethoxam, and dinotefuran.[26]

The majority of studies that measure toxicity of pesticides to Apis mellifera honeybees focus on estimating the lethal dose (LD50) in acute toxicity tests to adult honeybees. This is only a partial measure of the harmful effects that pesticides can have on bees. For a complete analysis of the impact of pesticides to bees, sublethal effects should be considered.[27]

Dozens of research articles have been published in peer-reviewed journals, which show sublethal effects to adult bees exposed to low levels of imidacloprid.[27] In these studies, sub-lethal doses of 1-24μg/kg and 0.1 - 20 ng/bee have been shown to impair navigation, foraging behavior, feeding behavior, and olfactory learning performance in honeybees (Apis mellifera).[23][28][29][30][31][32][33][34] Other studies examining higher levels of imidacloprid (50 - 500 ppb) also found that imidacloprid decreases foraging activity and affects bee mobility and communication capacity.[35][36][37]

A 2012 in situ study sought to recreate hypothesized conditions of the initial outbreak of CCD in 2006/2007 by feeding honey bees high fructose corn syrup (HFCS) that the researchers laced with varying sub-lethal amounts of imidacloprid assumed to have been present in HFCS feed at the time. All but one of the colonies exposed to imidacloprid perished between 13 and 23 weeks post imidacloprid dosing, providing evidence that long-term sub-lethal exposure to the neonicotinoid causes honey bees to exhibit symptoms consistent with CCD months after exposure.[15]

In 10-day chronic feeding studies with honeybees (Apis mellifera), 50% mortality was reached at levels between 0.1 and 10 ug/kg imidacloprid.[23] Other chronic toxicity studies conducted by Moncharmont et al. (2003) and Decourtye et al. (1999) have demonstrated chronic NOAEC values of <4 ppb and 4 ppb, respectively in honeybees.[38][39] In bumble bees, Mommaerts et al. (2009) demonstrated a LOAEC of 10 ppb for imidacloprid.[40]

Many tunnel and field studies have been conducted to show the potential effects of imidacloprid in the natural environment however most of these field studies have design and implementation deficiencies, which make them difficult to interpret and use.[8][26]